N-cadherin negatively regulates collective Drosophila glial migration through actin cytoskeleton remodeling

Journal of Cell Science

Volumn 128, Issue 5, 2015, Pages 900-912

  Kumar, Arun ^a,b,c,d,e   Gupta, Tripti ^a,b,c,d   Berzsenyi, Sara ^a,b,c,d,f   Giangrande, Angela ^a,b,c,d  

^a Institut de Géné tique et de Biologie Molé culaire et Cellulaire   (France)

^b CNRS   (France)

^c Institut National de la Santé et de la Recherche Médicale Inserm U964   (France)

^d UNIVERSITÉ DE STRASBOURG   (France)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f BIOTALENTUM LTD   (Hungary)

Author keywords

Actin cytoskeleton; Collective migration; Drosophila; Glial cells; N cadherin

Indexed keywords

ALPHA CATENIN; BETA CATENIN; NERVE CELL ADHESION MOLECULE; UVOMORULIN; CADHERIN; DROSOPHILA PROTEIN; N-CADHERIN PROTEIN, DROSOPHILA;

ACTIN FILAMENT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL MEMBRANE; CELL MIGRATION; CELL ULTRASTRUCTURE; CELLS BY BODY ANATOMY; CONTROLLED STUDY; DROSOPHILA; FORELIMB; GENE EXPRESSION; GLIA CELL; IN VIVO STUDY; MOLECULAR PHYLOGENY; NERVE CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; ANIMAL; CELL CULTURE; CELL MOTION; CYTOLOGY; CYTOSKELETON; DROSOPHILA MELANOGASTER; GENETICS; GLIA; HUMAN; METABOLISM; PHYSIOLOGY;

ALPHA CATENIN; ANIMALS; BETA CATENIN; CADHERINS; CELL MOVEMENT; CELLS, CULTURED; CYTOSKELETON; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; HUMANS; NEUROGLIA;

EID: 84924873756     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.157974     Document Type: Article

References (91)

1. Aigouy, B., Van de Bor, V., Boeglin, M. and Giangrande, A. (2004). Time-lapse and cell ablation reveal the role of cell interactions in fly glia migration and proliferation. Development 131, 5127-5138.
2. Aigouy, B., Lepelletier, L. and Giangrande, A. (2008). Glial chain migration requires pioneer cells. J. Neurosci. 28, 11635-11641.
3. Arikkath, J. and Reichardt, L. F. (2008). Cadherins and catenins at synapses: roles in synaptogenesis and synaptic plasticity. Trends Neurosci. 31, 487- 494.
4. Asano, K., Kubo, O., Tajika, Y., Huang, M. C., Takakura, K., Ebina, K. and Suzuki, S. (1997). Expression and role of cadherins in astrocytic tumors. Brain Tumor Pathol. 14, 27-33.
5. Asano, K., Kubo, O., Tajika, Y., Takakura, K. and Suzuki, S. (2000). Expression of cadherin and CSF dissemination in malignant astrocytic tumors. Neurosurg. Rev. 23, 39-44.
6. Bello, B. C., Izergina, N., Caussinus, E. and Reichert, H. (2008). Amplification of neural stem cell proliferation by intermediate progenitor cells in Drosophila brain development. Neural Dev. 3, 5.
7. Benjamin, J. M. and Nelson, W. J. (2008). Bench to bedside and back again: molecular mechanisms of alpha-catenin function and roles in tumorigenesis. Semin. Cancer Biol. 18, 53-64.
8. Berx, G. and van Roy, F. (2009). Involvement of members of the cadherin superfamily in cancer. Cold Spring Harb. Perspect. Biol. 1, a003129.
9. Berzsenyi, S. and Giangrande, A. (2010). Chain-like cell migration: a collective process conserved throughout evolution. Trends Dev. Biol. 4, 59-68.
10. Berzsenyi, S., Kumar, A. and Giangrande, A. (2011). Homeostatic interactions at the front of migration control the integrity and the efficiency of a migratory glial chain. J. Neurosci. 31, 13722-13727.
11. Blagg, S. L. and Insall, R. H. (2004). Solving the WAVE function. Nat. Cell Biol. 6, 279-281.
12. Brasch, J., Harrison, O. J., Honig, B. and Shapiro, L. (2012). Thinking outside the cell: how cadherins drive adhesion. Trends Cell Biol. 22, 299-310.
13. Brieher, W. M., Yap, A. S. and Gumbiner, B. M. (1996). Lateral dimerization is required for the homophilic binding activity of C-cadherin. J. Cell Biol. 135, 487- 496.
14. Cafferty, P. and Auld, V. J. (2007). No pun intended: future directions in invertebrate glial cell migration studies. Neuron Glia Biol. 3, 45-54.
15. Cai, D., Chen, S. C., Prasad, M., He, L., Wang, X., Choesmel-Cadamuro, V., Sawyer, J. K., Danuser, G. and Montell, D. J. (2014). Mechanical feedback through E-cadherin promotes direction sensing during collective cell migration. Cell 157, 1146-1159.
16. Caussinus, E., Colombelli, J. and Affolter, M. (2008). Tip-cell migration controls stalk-cell intercalation during Drosophila tracheal tube elongation. Curr. Biol. 18, 1727-1734.
17. Cayre, M., Canoll, P. and Goldman, J. E. (2009). Cell migration in the normal and pathological postnatal mammalian brain. Prog. Neurobiol. 88, 41-63.
18. Chu, Y. S., Eder, O., Thomas, W. A., Simcha, I., Pincet, F., Ben-Ze'ev, A., Perez, E., Thiery, J. P. and Dufour, S. (2006). Prototypical type I E-cadherin and type II cadherin-7 mediate very distinct adhesiveness through their extracellular domains. J. Biol. Chem. 281, 2901-2910.
19. Doyle, A. D., Petrie, R. J., Kutys, M. L. and Yamada, K. M. (2013). Dimensions in cell migration. Curr. Opin. Cell Biol. 25, 642-649.
20. Drees, F., Pokutta, S., Yamada, S., Nelson, W. J. and Weis, W. I. (2005). Alphacatenin is a molecular switch that binds E-cadherin-beta-catenin and regulates actin-filament assembly. Cell 123, 903-915.
21. El Sayegh, T. Y., Kapus, A. and McCulloch, C. A. (2007). Beyond the epithelium: cadherin function in fibrous connective tissues. FEBS Lett. 581, 167-174.
22. Foty, R. A. and Steinberg, M. S. (2004). Cadherin-mediated cell-cell adhesion and tissue segregation in relation to malignancy. Int. J. Dev. Biol. 48, 397- 409.
23. Fung, S., Wang, F., Chase, M., Godt, D. and Hartenstein, V. (2008). Expression profile of the cadherin family in the developing Drosophila brain. J. Comp. Neurol. 506, 469-488.
24. Galy, A., Schenck, A., Sahin, H. B., Qurashi, A., Sahel, J. A., Diebold, C. and Giangrande, A. (2011). CYFIP dependent actin remodeling controls specific aspects of Drosophila eye morphogenesis. Dev. Biol. 359, 37-46.
25. Gervais, L. and Casanova, J. (2011). The Drosophila homologue of SRF acts as a boosting mechanism to sustain FGF-induced terminal branching in the tracheal system. Development 138, 1269-1274.
26. Giagtzoglou, N., Ly, C. V. and Bellen, H. J. (2009). Cell adhesion, the backbone of the synapse: ''vertebrate'' and ''invertebrate'' perspectives. Cold Spring Harb. Perspect. Biol. 1, a003079.
27. Giangrande, A., Murray, M. A. and Palka, J. (1993). Development and organization of glial cells in the peripheral nervous system of Drosophila melanogaster. Development 117, 895-904.
28. Gilmour, D. T., Maischein, H. M. and Nü sslein-Volhard, C. (2002). Migration and function of a glial subtype in the vertebrate peripheral nervous system. Neuron 34, 577-588.
29. Godt, D. and Tepass, U. (2009). Breaking a temporal barrier: signalling crosstalk regulates the initiation of border cell migration. Nat. Cell Biol. 11, 536-538.
30. Goichberg, P., Shtutman, M., Ben-Ze'ev, A. and Geiger, B. (2001). Recruitment of beta-catenin to cadherin-mediated intercellular adhesions is involved in myogenic induction. J. Cell Sci. 114, 1309-1319.
31. Gupta, T. and Giangrande, A. (2014). Collective cell migration: ''all for one and one for all''. J. Neurogenet. 28, 190-198.
32. Halter, D. A., Urban, J., Rickert, C., Ner, S. S., Ito, K., Travers, A. A. and Technau, G. M. (1995). The homeobox gene repo is required for the differentiation and maintenance of glia function in the embryonic nervous system of Drosophila melanogaster. Development 121, 317-332.
33. Harris, T. J. and Tepass, U. (2010). Adherens junctions: from molecules to morphogenesis. Nat. Rev. Mol. Cell Biol. 11, 502-514.
34. Hegedü s, B., Marga, F., Jakab, K., Sharpe-Timms, K. L. and Forgacs, G. (2006). The interplay of cell-cell and cell-matrix interactions in the invasive properties of brain tumors. Biophys. J. 91, 2708-2716.
35. Iwai, Y., Usui, T., Hirano, S., Steward, R., Takeichi, M. and Uemura, T. (1997). Axon patterning requires DN-cadherin, a novel neuronal adhesion receptor, in the Drosophila embryonic CNS. Neuron 19, 77-89.
36. Iwai, Y., Hirota, Y., Ozaki, K., Okano, H., Takeichi, M. and Uemura, T. (2002). DN-cadherin is required for spatial arrangement of nerve terminals and ultrastructural organization of synapses. Mol. Cell. Neurosci. 19, 375-388.
37. Kiryushko, D., Berezin, V. and Bock, E. (2004). Regulators of neurite outgrowth: role of cell adhesion molecules. Ann. N. Y. Acad. Sci. 1014, 140-154.
38. Klämbt, C. (2009). Modes and regulation of glial migration in vertebrates and invertebrates. Nat. Rev. Neurosci. 10, 769-779.
39. Kobielak, A. and Fuchs, E. (2004). Alpha-catenin: at the junction of intercellular adhesion and actin dynamics. Nat. Rev. Mol. Cell Biol. 5, 614-625.
40. Kolotuev, I., Schwab, Y. and Labouesse, M. (2010). A precise and rapid mapping protocol for correlative light and electron microscopy of small invertebrate organisms. Biol. Cell 102, 121-132.
41. Koussa, M. A., Tolbert, L. P. and Oland, L. A. (2010). Development of a glial network in the olfactory nerve: role of calcium and neuronal activity. Neuron Glia Biol. 6, 245-261.
42. Kurusu, M., Katsuki, T., Zinn, K. and Suzuki, E. (2012). Developmental changes in expression, subcellular distribution, and function of Drosophila N-cadherin, guided by a cell-intrinsic program during neuronal differentiation. Dev. Biol. 366, 204-217.
43. Lee, B. P. and Jones, B. W. (2005). Transcriptional regulation of the Drosophila glial gene repo. Mech. Dev. 122, 849-862.
44. Lee, T. and Luo, L. (2001). Mosaic analysis with a repressible cell marker (MARCM) for Drosophila neural development. Trends Neurosci. 24, 251-254.
45. Lemke, G. (2001). Glial control of neuronal development. Annu. Rev. Neurosci. 24, 87-105.
46. Marín, O., Valiente, M., Ge, X. and Tsai, L. H. (2010). Guiding neuronal cell migrations. Cold Spring Harb. Perspect. Biol. 2, a001834.
47. Meyer, S., Schmidt, I. and Klämbt, C. (2014). Glia ECM interactions are required to shape the Drosophila nervous system. Mech. Dev. 133, 105-116.
48. Montell, D. J. (2003). Border-cell migration: the race is on. Nat. Rev. Mol. Cell Biol. 4, 13-24.
49. Montell, D. J., Yoon, W. H. and Starz-Gaiano, M. (2012). Group choreography: mechanisms orchestrating the collective movement of border cells. Nat. Rev. Mol. Cell Biol. 13, 631-645.
50. Murray, M. A., Schubiger, M. and Palka, J. (1984). Neuron differentiation and axon growth in the developing wing of Drosophila melanogaster. Dev. Biol. 104, 259-273.
51. Näthke, I. S., Hinck, L., Swedlow, J. R., Papkoff, J. and Nelson, W. J. (1994). Defining interactions and distributions of cadherin and catenin complexes in polarized epithelial cells. J. Cell Biol. 125, 1341-1352.
52. Nelson, W. J. (2008). Regulation of cell-cell adhesion by the cadherin-catenin complex. Biochem. Soc. Trans. 36, 149-155.
53. Niessen, C. M. and Gottardi, C. J. (2008). Molecular components of the adherens junction. Biochim. Biophys. Acta 1778, 562-571.
54. Nose, A., Nagafuchi, A. and Takeichi, M. (1988). Expressed recombinant cadherins mediate cell sorting in model systems. Cell 54, 993-1001.
55. Oda, H., Uemura, T., Shiomi, K., Nagafuchi, A., Tsukita, S. and Takeichi, M. (1993). Identification of a Drosophila homologue of alpha-catenin and its association with the armadillo protein. J. Cell Biol. 121, 1133-1140.
56. Orsulic, S., Huber, O., Aberle, H., Arnold, S. and Kemler, R. (1999). E-cadherin binding prevents beta-catenin nuclear localization and beta-catenin/LEF-1- mediated transactivation. J. Cell Sci. 112, 1237-1245.
57. Pacquelet, A. and Rørth, P. (2005). Regulatory mechanisms required for DEcadherin function in cell migration and other types of adhesion. J. Cell Biol. 170, 803-812.
58. Pai, L. M., Orsulic, S., Bejsovec, A. and Peifer, M. (1997). Negative regulation of Armadillo, a Wingless effector in Drosophila. Development 124, 2255-2266.
59. Pé glion, F. and Etienne-Manneville, S. (2012). N-cadherin expression level as a critical indicator of invasion in non-epithelial tumors. Cell Adh. Migr. 6, 327- 332.
60. Peifer, M., Sweeton, D., Casey, M. and Wieschaus, E. (1994). wingless signal and Zeste-white 3 kinase trigger opposing changes in the intracellular distribution of Armadillo. Development 120, 369-380.
61. Rappl, A., Piontek, G. and Schlegel, J. (2008). EGFR-dependent migration of glial cells is mediated by reorganisation of N-cadherin. J. Cell Sci. 121, 4089- 4097.
62. Rieger, S., Senghaas, N., Walch, A. and Kö ster, R. W. (2009). Cadherin-2 controls directional chain migration of cerebellar granule neurons. PLoS Biol. 7, e1000240.
63. Rimm, D. L., Koslov, E. R., Kebriaei, P., Cianci, C. D. and Morrow, J. S. (1995). Alpha 1(E)-catenin is an actin-binding and -bundling protein mediating the attachment of F-actin to the membrane adhesion complex. Proc. Natl. Acad. Sci. USA 92, 8813-8817.
64. Rørth, P. (2003). Communication by touch: role of cellular extensions in complex animals. Cell 112, 595-598.
65. Rørth, P. (2009). Collective cell migration. Annu. Rev. Cell Dev. Biol. 25, 407-429.
66. Rotty, J. D., Wu, C. and Bear, J. E. (2013). New insights into the regulation and cellular functions of the ARP2/3 complex. Nat. Rev. Mol. Cell Biol. 14, 7-12.
67. Sanson, B., White, P. and Vincent, J. P. (1996). Uncoupling cadherin-based adhesion from wingless signalling in Drosophila. Nature 383, 627-630.
68. Schenck, A., Bardoni, B., Langmann, C., Harden, N., Mandel, J. L. and Giangrande, A. (2003). CYFIP/Sra-1 controls neuronal connectivity in Drosophila and links the Rac1 GTPase pathway to the fragile X protein. Neuron 38, 887-898.
69. Schenck, A., Qurashi, A., Carrera, P., Bardoni, B., Diebold, C., Schejter, E., Mandel, J. L. and Giangrande, A. (2004).WAVE/SCAR, a multifunctional complex coordinating different aspects of neuronal connectivity. Dev. Biol. 274, 260-270.
70. Schwabe, T., Gontang, A. C. and Clandinin, T. R. (2009). More than just glue: the diverse roles of cell adhesion molecules in the Drosophila nervous system. Cell Adh. Migr. 3, 36-42.
71. Shan, W. S., Tanaka, H., Phillips, G. R., Arndt, K., Yoshida, M., Colman, D. R. and Shapiro, L. (2000). Functional cis-heterodimers of N- and R-cadherins. J. Cell Biol. 148, 579-590.
72. Shapiro, L. and Weis, W. I. (2009). Structure and biochemistry of cadherins and catenins. Cold Spring Harb. Perspect. Biol. 1, a003053.
73. Silies, M. and Klämbt, C. (2010a). APC/C(Fzr/Cdh1)-dependent regulation of cell adhesion controls glial migration in the Drosophila PNS. Nat. Neurosci. 13, 1357-1364.
74. Sofroniew, M. V. and Vinters, H. V. (2010). Astrocytes: biology and pathology. Acta Neuropathol. 119, 7-35.
75. Soustelle, L., Aigouy, B., Asensio, M. L. and Giangrande, A. (2008). UV laser mediated cell selective destruction by confocal microscopy. Neural Dev. 3, 11.
76. Stepniak, E., Radice, G. L. and Vasioukhin, V. (2009). Adhesive and signaling functions of cadherins and catenins in vertebrate development. Cold Spring Harb. Perspect. Biol. 1, a002949.
77. Stradal, T. E., Rottner, K., Disanza, A., Confalonieri, S., Innocenti, M. and Scita, G. (2004). Regulation of actin dynamics by WASP and WAVE family proteins. Trends Cell Biol. 14, 303-311.
78. Tepass, U., Truong, K., Godt, D., Ikura, M. and Peifer, M. (2000). Cadherins in embryonic and neural morphogenesis. Nat. Rev. Mol. Cell Biol. 1, 91-100.
79. Togashi, H., Sakisaka, T. and Takai, Y. (2009). Cell adhesion molecules in the central nervous system. Cell Adh. Migr. 3, 29-35.
80. Uchida, N., Honjo, Y., Johnson, K. R., Wheelock, M. J. and Takeichi, M. (1996). The catenin/cadherin adhesion system is localized in synaptic junctions bordering transmitter release zones. J. Cell Biol. 135, 767-779.
81. Utsuki, S., Sato, Y., Oka, H., Tsuchiya, B., Suzuki, S. and Fujii, K. (2002). Relationship between the expression of E-, N-cadherins and beta-catenin and tumor grade in astrocytomas. J. Neurooncol. 57, 187-192.
82. Valiente, M. and Marýn, O. (2010). Neuronal migration mechanisms in development and disease. Curr. Opin. Neurobiol. 20, 68-78.
83. Van De Bor, V., Walther, R. and Giangrande, A. (2000). Some fly sensory organs are gliogenic and require glide/gcm in a precursor that divides symmetrically and produces glial cells. Development 127, 3735-3743.
84. von Hilchen, C. M., Beckervordersandforth, R. M., Rickert, C., Technau, G. M. and Altenhein, B. (2008). Identity, origin, and migration of peripheral glial cells in the Drosophila embryo. Mech. Dev. 125, 337-352.
85. von Hilchen, C. M., Bustos, A. E., Giangrande, A., Technau, G. M. and Altenhein, B. (2013). Predetermined embryonic glial cells form the distinct glial sheaths of the Drosophila peripheral nervous system. Development 140, 3657- 3668.
86. Weber, G. F., Bjerke, M. A. and DeSimone, D. W. (2011). Integrins and cadherins join forces to form adhesive networks. J. Cell Sci. 124, 1183-1193.
87. Xiong, W. C., Okano, H., Patel, N. H., Blendy, J. A. and Montell, C. (1994). repo encodes a glial-specific homeo domain protein required in the Drosophila nervous system. Genes Dev. 8, 981-994.
88. Yamada, S., Pokutta, S., Drees, F., Weis, W. I. and Nelson, W. J. (2005). Deconstructing the cadherin-catenin-actin complex. Cell 123, 889- 901.
89. Yap, A. S., Brieher, W. M. and Gumbiner, B. M. (1997). Molecular and functional analysis of cadherin-based adherens junctions. Annu. Rev. Cell Dev. Biol. 13, 119-146.
90. Yonekura, S., Xu, L., Ting, C. Y. and Lee, C. H. (2007). Adhesive but not signaling activity of Drosophila N-cadherin is essential for target selection of photoreceptor afferents. Dev. Biol. 304, 759-770.
91. Zelhof, A. C. and Hardy, R. W. (2004). WASp is required for the correct temporal morphogenesis of rhabdomere microvilli. J. Cell Biol. 164, 417-426.